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Electron transport and photophosphorylation by Photosystem I in vivo in plants and cyanobacteria

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Abstract

Recently, a number of techniques, some of them relatively new and many often used in combination, have given a clearer picture of the dynamic role of electron transport in Photosystem I of photosynthesis and of coupled cyclic photophosphorylation. For example, the photoacoustic technique has detected cyclic electron transport in vivo in all the major algal groups and in leaves of higher plants. Spectroscopic measurements of the Photosystem I reaction center and of the changes in light scattering associated with thylakoid membrane energization also indicate that cyclic photophosphorylation occurs in living plants and cyanobacteria, particularly under stressful conditions.

In cyanobacteria, the path of cyclic electron transport has recently been proposed to include an NAD(P)H dehydrogenase, a complex that may also participate in respiratory electron transport. Photosynthesis and respiration may share common electron carriers in eukaryotes also. Chlororespiration, the uptake of O2 in the dark by chloroplasts, is inhibited by excitation of Photosystem I, which diverts electrons away from the chlororespiratory chain into the photosynthetic electron transport chain. Chlororespiration in N-starved Chlamydomonas increases ten fold over that of the control, perhaps because carbohydrates and NAD(P)H are oxidized and ATP produced by this process.

The regulation of energy distribution to the photosystems and of cyclic and non-cyclic phosphorylation via state 1 to state 2 transitions may involve the cytochrome b 6-f complex. An increased demand for ATP lowers the transthylakoid pH gradient, activates the b 6-f complex, stimulates phosphorylation of the light-harvesting chlorophyll-protein complex of Photosystem II and decreases energy input to Photosystem II upon induction of state 2. The resulting increase in the absorption by Photosystem I favors cyclic electron flow and ATP production over linear electron flow to NADP and ‘poises’ the system by slowing down the flow of electrons originating in Photosystem II.

Cyclic electron transport may function to prevent photoinhibition to the photosynthetic apparatus as well as to provide ATP. Thus, under high light intensities where CO2 can limit photosynthesis, especially when stomates are closed as a result of water stress, the proton gradient established by coupled cyclic electron transport can prevent over-reduction of the electron transport system by increasing thermal de-excitation in Photosystem II (Weis and Berry 1987). Increased cyclic photophosphorylation may also serve to drive ion uptake in nutrient-deprived cells or ion export in salt-stressed cells.

There is evidence in some plants for a specialization of Photosystem I. For example, in the red alga Porphyra about one third of the total Photosystem I units are engaged in linear electron transfer from Photosystem II and the remaining two thirds of the Photosystem I units are specialized for cyclic electron flow. Other organisms show evidence of similar specialization.

Improved understanding of the biological role of cyclic photophosphorylation will depend on experiments made on living cells and measurements of cyclic photophosphorylation in vivo.

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Abbreviations

CCCP:

carbonylcyanide m-chlorophenylhydrazone

cyt:

cytochrome

DBMIB:

2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone

DCCD:

dicyclohexylcarbodiimide

DCHC:

dicyclohexyl-18-crown-6

DCMU:

3-(3,4-dichlorophenyl)-1,1-dimethylurea

FCCP:

carbonylcyanide 4-(trifluoromethoxy) phenylhydrazone

LHC:

light harvesting chlorophyll

LHCP II:

light harvesting chlorophyll protein of Photosystem II

PQ:

plastoquinone

PS I, II:

Photosystem I, II

SHAM:

salicyl hydroxamic acid

TBT:

Tri-n-butyltin

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  1. Department of Plant Biology, Carnegie Institution of Washington, 290 Panama Street, 94305-1297, Stanford, CA, USA

    David C. Fork

  2. Department of Biological Science, University of Idaho, 83843, Moscow, ID, USA

    Stephen K. Herbert

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CIW/DPB Publication No. 1146

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Fork, D.C., Herbert, S.K. Electron transport and photophosphorylation by Photosystem I in vivo in plants and cyanobacteria. Photosynth Res 36, 149–168 (1993). https://doi.org/10.1007/BF00033035

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